Abstract

Our movements are shaped by our perception of the world as communicated by our senses. Perception of sensory information has been largely attributed to cortical activity. However, a prior level of sensory processing occurs in the spinal cord. Indeed, sensory inputs directly project to many spinal circuits, some of which communicate with motor circuits within the spinal cord. Therefore, the processing of sensory information for the purpose of ensuring proper movements is distributed between spinal and supraspinal circuits. The mechanisms underlying the integration of sensory information for motor control at the level of the spinal cord have yet to be fully described. Recent research has led to the characterization of spinal neuron populations that share common molecular identities. Identification of molecular markers that define specific populations of spinal neurons is a prerequisite to the application of genetic techniques devised to both delineate the function of these spinal neurons and their connectivity. This strategy has been used in the study of spinal neurons that receive tactile inputs from sensory neurons innervating the skin. As a result, the circuits that include these spinal neurons have been revealed to play important roles in specific aspects of motor function. We describe these genetically identified spinal neurons that integrate tactile information and the contribution of these studies to our understanding of how tactile information shapes motor output. Furthermore, we describe future opportunities that these circuits present for shedding light on the neural mechanisms of tactile processing.

Demonstration of a genetically identified spinal circuit integrating tactile input for motor control. A: scheme of isolated in vitro spinal cord preparation with sural nerve left in continuity used to test for the presence of reflexes evoked by stimulation of tactile inputs. Stimulating electrodes (red) were placed on the sural nerve, which is predominantly cutaneous, and the mixed sensory tibial nerve distal to the sural nerve branchpoint. Recording suction electrodes (green) were placed on the ipsilateral lumbar L5 dorsal (sensory) and L5 ventral (motor) roots. B: to demonstrate the predominantly cutaneous nature of the sural nerve, electroneurogram (ENG) recordings of L5 dorsal root potentials (DRPs), in response to sural nerve or tibial nerve stimulations, were made. In this example, note the longer latency of the sural nerve DRP compared with the tibial nerve DRP, which is due to the proprioceptive component of the tibial nerve. Furthermore, the threshold to evoke a DRP was higher for sural nerve [cutaneous (cut.) DRP; 3 μA] than tibial nerve [proprioceptive (proprio.) DRP; 2 μA] stimulation. C: to test for motor reflexes in response to stimulation of cutaneous afferents, ENG recordings of L5 ventral root responses to multiple stimulation pulses applied to the sural nerve were made. A putative disynaptic reflex response, highlighted in the dashed box, can be observed in control mice but not in animals that had dI3 INs genetically silenced (dI3OFF). D: diagram of experimental design used to test for the presence of motor reflexes evoked by tactile inputs conveyed by the sural nerve and mediated by dI3 INs. Chronically implanted electrodes into gastrocnemius and tibialis anterior muscles of adult control and dI3OFF mice enabled electromyographic (EMG) recordings in awake, behaving mice. E: similar to in vitro tests, EMG recordings of gastrocnemius to multiple stimulation pulses applied to the sural nerve show a putative disynaptic reflex response (dashed box) that is absent in dI3OFF mice. F: diagram representing dI3 INs (dI3) as part of a disynaptic pathway among SNs that are LTMRs, dI3 INs, and motoneurons (MN) [adapted from with permission from Elsevier]. DRG, dorsal root ganglion.

Conceptual model of sensorimotor neural processing in the spinal cord. Proposed scheme in which sensory inputs from multiple modalities are conveyed in parallel to partially overlapping spinal IN populations. The converging sensory information is processed, and sets of instructive motor commands are generated. These commands diverge to motor modules that generate individual motor actions, which together, form the desired coordinated motor response. We propose that this anatomical and functional structure provides a biological framework to neuronal computations underlying spinal sensorimotor integration.